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The Role of Plantigrady and Heel-Strike in the Mechanics and Energetics of Human Walking with Implications for the Evolution of the Human Foot James T

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The Role of Plantigrady and Heel-Strike in the Mechanics and Energetics of Human Walking with Implications for the Evolution of the Human Foot James T © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 RESEARCH ARTICLE The role of plantigrady and heel-strike in the mechanics and energetics of human walking with implications for the evolution of the human foot James T. Webber* and David A. Raichlen ABSTRACT mid- or forefoot contact. Given the importance of limb length to Human bipedal locomotion is characterized by a habitual heel-strike cursorial mammals, it is uncertain why humans use a plantigrade (HS) plantigrade gait, yet the significance of walking foot-posture is foot posture with a consistent HS during walking (Cunningham not well understood. To date, researchers have not fully investigated et al., 2010). the costs of non-heel-strike (NHS) walking. Therefore, we examined A popular hypothesis is that the human HS gait evolved to reduce walking speed, walk-to-run transition speed, estimated locomotor the energy costs of walking (Cunningham et al., 2010; Usherwood costs (lower limb muscle volume activated during walking), impact et al., 2012). This hypothesis is supported by studies showing transient (rapid increase in ground force at touchdown) and effective subjects had relatively high energy costs of locomotion (COL) when limb length (ELL) in subjects (n=14) who walked at self-selected asked to walk with digitigrade foot postures compared with typical speeds using HS and NHS gaits. HS walking increases ELL plantigrade HS walking (Cunningham et al., 2010). Yet, human compared with NHS walking since the center of pressure translates lower limb anatomy is not adapted for full digitigrady and it is anteriorly from heel touchdown to toe-off. NHS gaits led to decreased possible that these experiments captured the energetic costs of novel absolute walking speeds (P=0.012) and walk-to-run transition speeds gaits. Non-human apes may offer more context into how and why (P=0.0025), and increased estimated locomotor energy costs habitual HS walking evolved in humans because we often assume (P<0.0001) compared with HS gaits. These differences lost that traits shared among apes may have been present in our pre- significance after using the dynamic similarity hypothesis to bipedal ancestors. Extant non-human apes use an array of account for the effects of foot landing posture on ELL. Thus, plantigrade walking gaits, some of which lack consistent heel reduced locomotor costs and increased maximum walking speeds strikes (Schmitt and Larson, 1995). For example, researchers have in HS gaits are linked to the increased ELL compared with NHS shown that our closest living relatives, bonobos (Pan paniscus) and gaits. However, HS walking significantly increases impact transient common chimpanzees (Pan troglodytes), use a wide range of values at all speeds (P<0.0001). These trade-offs may be key to landing postures, from a traditional human-like heel strike, to understanding the functional benefits of HS walking. Given the landings where the heel does not touch down until the second half of current debate over the locomotor mechanics of early hominins and stance phase (see Elftman and Manter, 1935; Vereecke et al., 2003). the range of foot landing postures used by nonhuman apes, we Most often, these apes use gaits where the heel and mid-foot contact suggest the consistent use of HS gaits provides key locomotor the ground simultaneously, which also differ from human HS advantages to striding bipeds and may have appeared early in walking where initial ground contact is made by the heel alone hominin evolution. (Elftman and Manter, 1935; Vereecke et al., 2003). Thus, the key human evolutionary shift from the non-hominin ape foot landings KEY WORDS: Bipedalism, Heel-strike, Limb length, Locomotion, appears to be the consistent use of heel-only landing postures. Australopithecus sediba, Homo floresiensis The goal of this study is to better understand the advantages and disadvantages of this shift to consistent HS gaits. To accomplish this INTRODUCTION goal, we measured the mechanics and energetics of human walking Plantigrady is rare among cursorial mammals (Hildebrand and with the two footfall extremes seen in ape-like plantigrade walking: Goslow, 1998), which typically utilize digitigrade or unguligrade an HS, where touchdown occurs with the heel only, and a non-heel gaits to maximize limb length, which is a key determinant of the strike (NHS), where initial ground contact occurs at mid-foot and energetic cost of locomotion (Hildebrand and Goslow, 1998; Kram the heel lands later in stance. Interestingly, although humans do not and Taylor, 1990; Pontzer, 2007a). Humans represent an exception habitually walk with either digitigrade or more ape-like gaits, to this pattern (Cunningham et al., 2010) as we possess adaptations Lieberman et al. (2010) found that many individuals adopt NHS for endurance terrestrial running (Bramble and Lieberman, 2004; gaits at running speeds, similar to those used at times by nonhuman Carrier, 1984), combined with plantigrade feet and a prominent heel apes. Running with an HS foot posture produces rapid and strike (HS), during walking gaits, where the foot touches down heel potentially dangerous increases in the ground reaction force first on the calcaneal tuberosity in a dorsiflexed posture, without (GRF), known as an impact transient (IT), just after the heel impacts the ground (Lieberman et al., 2010). NHS footfalls seem to School of Anthropology, University of Arizona, Tucson, AZ 85721, USA. benefit runners by reducing ITs at higher locomotor speeds (Lieberman et al., 2010), possibly decreasing injury rates *Author for correspondence ([email protected]) (Lieberman, 2012) without increasing locomotor costs (Divert J.T.W., 0000-0002-5354-9457 et al., 2005, 2008; Franz et al., 2012; Kram and Franz, 2012). By specifically exploring the possible benefits of using an HS at slow Received 5 February 2016; Accepted 18 September 2016 locomotor speeds, we hope to better understand why a consistent Journal of Experimental Biology 3729 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3729-3737 doi:10.1242/jeb.138610 A List of symbols and abbreviations COL cost of locomotion COP center of pressure COPc change in center of pressure (m) DC dynamically calculated DSH dynamic similarity hypothesis _ 3 −1 NHS ECOL estimated cost of locomotion (cm Ns ) HS ELL effective limb length (m) Fmusc muscle force Fr Froude number Fr′ plantigrade adjusted Froude number GRF ground reaction force (N) B C HS heel-strike COPc IT impact transient d d 1 2 lfasc muscle fascicle length L limb length (m) L′ plantigrade adjusted limb length (m) θ θ M moment 1 2 NHS non-heel-strike t foot contact time (s) c LЈ 3 −1 Vmusc volume of active muscle (cm N ) WTR walk-to-run HS evolved in our bipedal ancestors, and whether NHS gaits offer any advantages that may explan their occasional use in other apes. Fig. 1. Differences in posture and limb length in heel-strike (HS) and non- heel-strike (NHS) gaits. (A) Examples of foot posture at initial touchdown, HS Plantigrade walking and effective limb length and NHS. Dashed line indicates surface. (B) Depiction of L′, effective limb As noted by Cunningham et al. (2010), human use of plantigrade length (m), modeled as a point mass on the end of a rigid limb, taking into foot postures is unique among organisms adapted for long distance consideration COPc, the translation in COP during stance and hip excursion angle θ. (C) Depiction of L′ added limb length (region circled in B), see travel since plantigrady reduces hindlimb length compared with Materials and methods for details. digitigrade postures. Limb length is a key determinant of walking mechanics and energetics because when modeled as an inverted pendulum, the limb acts as a strut during stance phase, with the humans, many of the foot postures used by nonhuman apes lead to center of mass vaulting over the point of ground contact (Alexander, reduced total translation of the COP (Vereecke et al., 2003). For 1976; Gray, 1944; Kuo, 2001; Pontzer, 2005). Long limbs reduce example, when bonobos land on both the heel and midfoot energy costs in this model by increasing step lengths, which leads to simultaneously (Elftman and Manter, 1935; Vereecke et al., 2003, longer time periods for accelerating the center of mass and reduced 2005), the COP originates between the heel and forefoot, rather than rates of force generation (Pontzer, 2007a). directly under the heel. Therefore, a consistent HS landing posture Characterizing the effects of plantigrade HS walking on the that maximizes COP translation may be a novel evolutionary length of the pendulum strut may help to explain why this footfall solution to lengthening inverted pendulum struts from an ape-like pattern evolved. Researchers typically use either a linear sum of ancestral condition. skeletal elements (Steudel and Beattie, 1995), the height of the hip We use the dynamic similarity hypothesis (DSH) to test this in quiet stance (Pontzer, 2007a) or hip height at mid-stance during model of inverted pendulum strut length. The DSH suggests that locomotion to describe effective limb length (ELL: average length the motions of two animals are comparable if they can be made of the strut over a step). These lengths assume the pivot point of the similar through dimensional scaling (Alexander and Jayes, 1983). inverted pendulum is fixed at ground contact and therefore Dimensionless parameters can be compared at speeds where the plantigrady should reduce ELL compared with digitigrade foot ratios of inertial to gravitational forces acting on two moving postures. However, the pivot point translates anteriorly during a step systems are equal. This condition is met when organisms walk at the [i.e. the center of pressure (COP) shifts continuously throughout the same Froude number (Fr; Alexander, 1989): stance phase] in plantigrade walkers.
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